Predation by Nesidiocoris Tenuis on Bemisia Tabaci and Injury to Tomato

BioControl (2009) 54:237–246 DOI 10.1007/s10526-008-9164-y

Predation by Nesidiocoris tenuis on Bemisia tabaci and injury to tomato

Javier Calvo Æ Karel Bolckmans Æ Philip A. Stansly Æ Alberto Urbaneja

Received: 16 January 2007 / Accepted: 14 April 2008 / Published online: 10 May 2008 Ó International Organization for Biological Control (IOBC) 2008

Abstract Tomato is the most important vegetable considered a pest because it can feed on tomato crop in Spain. The mirid bug Nesidiocoris tenuis plants, causing necrotic rings on stems and flowers (Reuter) commonly appears in large numbers in and punctures in fruits. Our objectives were to protected and open-air tomato crops where little or no evaluate predation by N. tenuis on sweetpotato broad-spectrum insecticides are used. Nesidiocoris whitefly Bemisia tabaci Gennadius under greenhouse tenuis is known to be a predator of whiteflies, thrips conditions and establish its relationship to N. tenuis and several other pest species. However, it is also feeding on tomato. Two different release rates of N. tenuis were compared with an untreated control (0, 1 and 4 N. tenuis plant-1) in cages of 8 m2. Hanlding editor: Eric Lucas. Significant reductions of greater than 90% of the whitefly population and correspondingly high num- This research is part of an internal R&D project conducted at bers of N. tenuis were observed with both release Koppert Biological Systems S.L. in Spain. The main goal was rates. Regression analysis showed that necrotic rings to improve control of Bemisia tabaci in protected crops of southeastern Spain by bringing on a new biological control on foliage caused by N. tenuis were best explained by agent. the ratio of B. tabaci nymphs:N. tenuis as predicted by the equation y = 15.086x - 0.6359. J. Calvo Á A. Urbaneja R & D Department, Koppert Biological Systems S.L., Finca Labradorcico del Medio, s/n. Apartado de Correos Keywords Miridae Á Whitefly Á Biological control Á 286, 30880 Aguilas, Spain Zoophytophagy

K. Bolckmans R & D Department, Koppert B.V., Veilingweg 17, 2651 BE Berkel en Rodenrijs, The Netherlands Introduction

P. A. Stansly Tomato (Lycopersicon esculentum Mill.) is the most University of Florida-IFAS, 2686 State Road 29N, important vegetable crop in Spain, with a production 34142 Immokalee, FL, USA area of close to 60,000 ha in 2002 and a total A. Urbaneja (&) production of 4 million metric tonnes. Almost 28% Unidad de Entomologıá, Centro de Proteccioń Vegetal y of this volume is produced in the Comunidad Biotecnologıá, Instituto Valenciano de Investigaciones Autońoma de Murcia and in the adjacent province Agrarias (IVIA), Carretera de Moncada – Na´quera Km. 4,5, 46 113 Moncada, Valencia, Spain of Almerıá (INE 2002). In both regions, tomatoes are e-mail: [email protected] grown primarily in plastic covered greenhouses. In 123 238 J. Calvo et al. recent years, the most harmful pest of tomato in these et al. 1976; Kajita 1978; Malausa 1989; Malausa and regions has been the whitefly Bemisia tabaci (Gen- Henao 1988; Vacante and Grazia 1994). The necrotic nadius) (Hem.: Aleyrodidae). This pest causes rings on the flower petiole can result in under certain damage by sucking the sap, thus weakening the conditions on floral abortion (Calvo and Urbaneja plant, and by secreting large amounts of honeydew 2004;Sańchez et al. 2006). Intensity of injury to that favour the appearance of sooty mould. However, tomato has been observed to decrease with increased the greatest impact on tomato is due to its role as availability of prey (Arno´ et al. 2006). vector of tomato yellow leaf curl virus (TYLCV) The aim of the present work is to evaluate the (SIFA 2004). Serious economic losses have been efficacy of N. tenuis in controlling B. tabaci and to caused in Spain by this geminivirus since its appea- characterize damage to tomato. This information could rance in the 1990s (CARM 1996). Consequently, then form a basis for management of N. tenuis that will permissible population levels of B. tabaci are mini- optimize benefits derived from predation on B. tabaci mal, such that implementation of biocontrol based while minimizing damage to the tomato crop. IPM programs is difficult (Stansly et al. 2004). Nevertheless, interest in biological control continues to increase in Spain (Castan˜e´ 2002; van der Blom Materials and methods 2002), thanks in part to adaptation of TYLCV- tolerant varieties, development of pesticide resistance Test facilities (Cahill et al. 1996; Elbert and Nauen 2000) and successful use of natural enemies against this pest The experiment was conducted in a 40 9 10 m air (Stansly et al. 2004, 2005a, b; Urbaneja et al. 2002; inflated double layered polyethylene covered Quonset Calvo and Belda 2006). style greenhouse equipped with pad-and-fan cooling The parasitoid Eretmocerus mundus Mercet (Hym.: and diesel-fired heating, located at the Koppert Aphelinidae) and the predator Nesidiocoris tenuis Biological Systems S.A. facilities in A´ guilas, Murcia, Reuter (Hem.: Miridae) (Sańchez et al. 2003a, b; van Spain. The plastic tunnel was accessed through a der Blom 2002) are endemic natural enemies of double door and was divided into 36 experimental B. tabaci that commonly appear in tomato crops in cages constructed of ‘‘anti-thrips’’ polyethylene Southern Spain. The biology, behaviour and effec- screening with 220 9 331 lm interstices supported tiveness of E. mundus is well documented (Stansly by heavy guy wires connected to the greenhouse et al. 2004, 2005a, b; Urbaneja and Stansly 2004), and superstructure. Each experimental cage was 4 9 2 9 this parasitoid is mass-reared and released to control 3.5 m (l 9 w 9 h) and covered on the floor with a B. tabaci in greenhouse vegetable crops in this region 2 mm-thick woven white polyethylene ground cloth. (Urbaneja et al. 2003a). In contrast, only limited Each cage was accessed by an independent door research has been reported on the potential of N. tenuis secured with a zipper. Twelve cages were used for the for augmentative biological control of B. tabaci. present study, six on either side of the centre aisle. Often cited with regard to its polyphagous habit Dataloggers (model HOBO H8 RH/Temp, Onset (Goula 1985; Urbaneja et al. 2005) or zoophytopha- Computer Company, Bourne, MA, the USA) were gous behaviour (Dolling 1991), N. tenuis has been placed in four different cages to record temperature observed to contribute to the control of whiteflies, and relative-humidity. thrips, leafminers, spidermites, and Lepidoptera species in greenhouses (Arzone et al. 1990; Calvo and Environmental conditions Urbaneja 2003; Carnero et al. 2000; Marcos and Rejesus 1992; Solsoloy et al. 1994; Torreno 1994; The average temperature during the experiment ranged Trottin-Caudal and Millot 1997; Vacante and between 26°C, on 3 October 2002, to 20°C, on 16 Benuzzi 2002; Vacante and Grazia 1994). However, January 2003, with an absolute minimum and maximum N. tenuis has also been classified as a pest of tomato of 14.5 and 38.3°C respectively during the test period (Male´zieux et al. 1995) due to feeding damage such (Fig. 1A). Average relative humidity ranged from 84%, as necrotic rings in both leaf and flower petioles, and on 31 October 2002 to 65% on 16 January 2003 with whitish halos on fruit (Arno´ et al. 2006; El-Dessouki absolute values of 100 and 22% respectively (Fig. 1B). 123 Predation by Nesidiocoris tenuis on Bemisia tabaci 239

Fig. 1 A Temperature ( ) A 40 and relative humidity (B)in the greenhouse during the experiment 30 C) ° 20 Temp (

0 123456789101112131415 Trial Week Mean Max Min

B 100

RH (%) 40

0 123456789101112131415 Trial Week

Mean Max Min

Plant and pest management other plant, densities. Crop cultivation techniques typical of tomato greenhouse-cultivation in Spain Tomato seeds variety ‘Boludo’, tolerant to TYLCV were followed: a trellis of two wire-guides for each and TSWV (Seminis Vegetable Seeds Europe plant to which the main stem was trained using black Enkhuizen, The Netherlands), were sown on 1 polyethylene string, weekly pruning of secondary September 2002. Seeds were deposited in 5.4 cm2 shoots, application of a standard nutrient solution for cells in expanded polystyrene trays of 11 9 19 cm tomato by means of an automated-irrigation system filled with peat. On 27 September, seedlings were with an irrigation frequency adjusted to accumulated transplanted into polyethylene 6.3 l flowerpots filled radiation (800 W m-2), and an irrigation time of with cocopeat (coir) growing medium and placed 8.5 min. inside the experimental greenhouse in two rows of 5 plants per cage or 1.25 plants m-2. Plant densities in Whiteflies and predators commercial tomato crops in southern Spain vary from 1.25 to 3 plants m-2. However therefore, the release Bemisia tabaci adults came from an experimental rates for all the insects were calculated in individuals colony located in A´ guilas and identified as B. tabaci per plant, so results could easily be transformed to biotype ‘‘Q’’ based on DNA analysis (J.L. Cenis, 123 240 J. Calvo et al.

IMIDA La Alberca. Murcia, Espanã, Personal adults, and necrotic rings during the course of the trial Communication). Less than 4-day-old N. tenuis were calculated (Stansly et al. 2005a, b). The resulting adults were obtained from an experimental colony estimates of insect and damage accumulated 9 days maintained at 25°C and 75% RH, maintained on (= area under the weekly incidence curve) was then tobacco plants and fed with Ephestia kuehniella subjected to a one-way analysis of variance joined with Zeller (Lepidoptera: Pyralidae) eggs. The sex-ratio of a Tukey’s test for mean separation (P \ 0.05). this colony was 0.5 female/total. The colony origi- The number of necrotic rings per leaf was fitted to nated from specimens collected during summer 2002 the number of B. tabaci nymphs per leaf, the number in tomato greenhouses in the province of Murcia. of N. tenuis individuals (adults and nymphs) per leaf and the ratio of B. tabaci nymphs per leaf:number of Experimental design N. tenuis adults + nymphs per leaf using linear, power, exponential, inverse and logarithmic regres- Three release rates of N. tenuis were compared in the 12 sion analyses. All statistical analyses were carried out cages using a randomized complete block design with with SPSS v12.0 (SPSS 2004). three treatments replicated four times. The three treat- -1 ments were a one time release of 1 or 4 N. tenuis plant Results plus a control receiving no release. One N. tenuis per plant is the recommended release rate (Calvo and Bemisia tabaci populations Urbaneja 2004), so the aim of the higher rate was to test effects of an excessive number of predators. The greatest number of whitefly adults per leaf Each cage was infested with 55 adult B. tabaci on (93.1 ± 24.7) were observed in the control treatment October 3rd, 2002, one week before the first evalua- the last week of the test (Fig. 2A). This compared to a tion. The infestation of 55 adult whiteflies per cage was maximum of 17.4 ± 5.0 adults per leaf observed in chosen to simulate a strong and early whitefly attack. week 12 in cages receiving 1 N. tenuis plant-1, Two weeks later (just after the second evaluation), representing a relative reduction of 81%. The N. tenuis was released inside the cages. Special care maximum number of B. tabaci adults in cages was always taken to enter the control cages first, then receiving 4 N. tenuis plant-1, observed in week 9, the cages with the lower release rate and finally the was only 3.3 ± 0.6, representing a 96% reduction ones with the higher release rate, to reduce risk of compared to the maximum in the control treatment. accidental contamination among treatments. Accumulated B. tabaci adult per day reflected these relationships although differences between the 1 and Evaluations 4 N. tenuis plant-1 release rates were not significantly different (F = 43.16; d.f. = 2, 53; P \ 0.001) Six randomly chosen plants per cage were sampled (Table 1). weekly for 15 weeks, beginning 10 October, 2002. Similar trends were observed in numbers of First, the number of N. tenuis nymphs and adults and B. tabaci nymphs, with maxima at the end of the the number of necrotic rings were counted from 7 experiment reaching 744.5 ± 116.1, 297.0 ± 89.2 and apical leaves of the 6 plants (Castan˜e´ and Carnero 92.9 ± 12.6 for the control treatment, and the 1 and 4 2002). Then a leaf belonging to the middle strata was N. tenuis plant-1 treatments respectively representing selected at random from each plant and cautiously reductions of 62% and 87% respectively (Fig. 2B). turned to count the number of B. tabaci adults. Finally Again, the number of accumulated nymph per day was nymphs (N1–N4) were counted on this same leaf using significantly different between the control and the two a109 hand lens (Stansly et al. 2005a). release rates with no differences between the latter (F = 28.94; d.f. = 2, 53; P \ 0.001) (Table 1). Statistical analysis Nesidiocoris tenuis populations Values are expressed as mean ± standard error of the mean. The accumulated number of whitefly nymphs Most adult N. tenuis were initially observed in cages plus pupae, whitefly adults, N. tenuis nymphs and receiving the high release rate. However, their numbers 123 Predation by Nesidiocoris tenuis on Bemisia tabaci 241

Fig. 2 Average whiteﬂy 125 adults (A) and nymphs (B) A per leaf in each week (±SE) for treatments receiving 0, 1 100 and 4 N. tenuis plant-1. Whiteﬂies were released in 75 week 0 and N. tenuis was

released just after the Adults / leaf second evaluation in week 2 50

B. tabaci B. 25

0 123456789101112131415 Trial Week 0 Nt/pl 1 Nt/pl 4 Nt/pl

900 B 750

600

450

300

B. tabaci Nymphs / leaf / Nymphs tabaci B. 150

0 123456789101112131415 Trial Week 0 Nt/pl 1 Nt/pl 4 Nt/pl

Table 1 Average nymphs Release rate (Ind. plant-1) and adults of B. tabaci (±SE), nymphs and adults 0 N. tenuis plant-1 1 N. tenuis plant-1 4 N. tenuis plant-1 of N. tenuis (±SE) and necrotic rings (±SE) B. tabaci accumulated per day for Adults 2360.4 ± 251.4 a 741.4 ± 164.1 b 161.0 ± 13.0 b treatments receiving 0, 1 and 4 N. tenuis per plant Nymphs 32795.2 ± 4573.5 a 10732.6 ± 1821.0 b 3339.0 ± 338.0 b N. tenuis Means in the same row Adults 5.0 ± 1.03 b 25.2 ± 1.9 a 31.0 ± 1.8 a followed by the same letter Nymphs 7.5 ± 1.4 c 31.4 ± 2.0 b 57.2 ± 2.4 a are not signiﬁcant different Necrotic rings 12.6 ± 2.1 c 56.7 ± 3.1 b 88.2 ± 3.1 a (Tukey, P \ 0.05) declined after week 11 compared to low release cages 4 N. tenuis plant-1 release rate (Fig. 3B). Furthermore, (Fig. 3A) although differences in number of accumu- more cumulative nymphs per day were observed with lated adults per day did not differ signiﬁcantly between 4 N. tenuis plant-1 compared to 1 N. tenius plant-1 the two release rates (F = 70.52; d.f. = 2, 251; (Table 1)(F = 157.61; d.f. = 2, 251; P \ 0.001). As P \ 0.001) (Table 1). Peak numbers of mirid nymphs many as 0.2 ± 0.1 adults and 0.4 ± 0.1 nymphs per were considerably greater in response to the terminal were seen in cages where no N. tenuis were

123 242 J. Calvo et al.

Fig. 3 Average 1,5 Nesidiocoris tenuis adults A (A) and nymphs (B) per leaf in each week (±SE) for treatments receiving 0, 1 and 4 N. tenuis plant-1. 1,0 Whiteﬂies were released in week 0 and N. tenuis was released just after the Adults / leaf second evaluation in week 2 0,5 N. tenuisN.

0,0 1 2 3 4 5 6 7 8 9 101112131415 Trial Week 0 Nt/pl 1 Nt/pl 4 Nt/pl

2,0 B

1,5

1,0 Nymphs leaf /

0,5 N. tenuis N.

0,0 123456789101112131415 Trial Week 0 Nt/pl 1 Nt/pl 4 Nt/pl released due to unintentional contamination, although R2 and F values were highest using power regression. fewer N. tenuis day-1 were accumulated in these cages The regression equation was y = 15.086x - 0.6359, compared to release cages. where y was the number of necrotic rings per leaf and x was the ratio of B. tabaci nymphs to N. tenuis Plant injury adults + nymphs (Fig. 5).

The first necrotic rings were observed in week 6 with the greatest incidence always in cages receiving Discussion 4 N. tenuis plant-1 (Fig. 4). Maxima observed per leaf were 3.9 ± 0.2, 1.6 ± 0.1and 0.5 ± 0.1 for Nesidiocoris tenuis was highly effective in control- the high, low and zero release rates respectively. ling B. tabaci on tomato under these experimental Differences were significant among all treatments in conditions, with little difference observed between the number of accumulated necrotic rings day-1 the two release rates evaluated. Whitefly reductions (Table 1)(F = 181.67; d.f. = 2, 251; P \ 0.001). of up 81% and 96% were recorded with only one Regression analysis showed best fit between release of 1 or 4 N. tenuis plant-1 respectively. number of necrotic rings and the ratio of B. tabaci Furthermore, N. tenuis established well in the tomato nymphs to N. tenuis adults + nymphs (Table 2). crop under the experimental conditions, reaching 123 Predation by Nesidiocoris tenuis on Bemisia tabaci 243

Fig. 4 Average necrotic 5 rings per leaf in each week (±SE) for treatments receiving 0, 1 and 4 4 N. tenuis plant-1. Whiteﬂies were released in 3 week 0 and N. tenuis was released just after the second evaluation in week 2 2

Necrotic Rings / Leaf / Rings Necrotic 1

0 123456789101112131415 Trial Week 0 Nt/pl 1 Nt/pl 4 Nt/pl

Table 2 Lineal, power, Curve type R2 d.f. FPa b exponential, inverse and logarithmic regression Necrotic rings depending on the number of nymphs of B. tabaci/N. tenuis analysis of the number of necrotic rings observed with Lineal 0.191 53 12.288 0.001 -0.001 ± 0.000 1.647 ± 0.149 the number of B. tabaci Logarithmic 0.705 53 124.270 \0.001 -0.630 ± 0.057 4.163 ± 0.259 nymphs per leaf, with the Inverse 0.675 53 107.914 \0.001 26.867 ± 2.586 0.651 ± 0.113 number of N. tenuis Power 0.745 53 151.842 \0.001 -0.636 ± 0.052 15.086 ± 3.565 individuals (adults and pupae) per leaf and with the Exponential 0.351 53 28.101 \0.001 -0.001 ± 0.000 1.278 ± 0.168 quotient B. tabaci nymphs Necrotic rings depending on the number of nymphs of B. tabaci per leaf/individuals of Lineal 0.308 53 23.139 \0.001 -0.005 ± 0.001 1.994 ± 0.172 N. tenuis per leaf Logarithmic 0.477 53 47.473 \0.001 -0.761 ± 0.110 4.675 ± 0.484 Inverse 0.297 53 21.953 \0.001 26.289 ± 5.611 0.846 ± 0.176 Power 0.350 53 27.959 \0.001 -0.640 ± 0.121 14.617 ± 7.750 Exponential 0.257 53 18.021 \0.001 -0.004 ± 0.001 1.587 ± 0.278 R2 is the r square parameter; Necrotic rings depending on the number of N. tenuis d.f. are the degrees Lineal 0.543 53 61.674 \0.001 1.295 ± 0.165 -0.90 ± 0.218 freedom; F is the Fisher’s Logarithmic 0.418 53 37.278 \0.001 0.849 ± 0.139 1.488 ± 0.115 parameter; P is the significant level and a and b Inverse 0.187 53 11.926 0.001 -0.164 ± 0.048 1.720 ± 0.160 are the constant and the Power 0.649 53 96.348 \0.001 1.040 ± 0.106 1.028 ± 0.090 dependent parameter of the Exponential 0.584 53 73.129 \0.001 1.320 ± 0.154 0.203 ± 0.041 curve (±SE) high population levels with both release rates Macrolophus pygmaeus Rambur and Dicyphus assayed. These results are consistent with studies tamaninii Wagner (Het.: Miridae), were able to reach showing that tomato plants are good host plants for adulthood feeding on tomato leaves and fruits, N. tenuis (Carnero et al. 2000; El-Dessouki et al. respectively (Perdikis and Lykouressis 2000; Lucas 1976; Goula 1985; Goula and Alomar 1994;Sańchez and Alomar 2001). et al. 2003a, b; Urbaneja et al. 2005). In the present experiment, the number of accumu- We found in an earlier study that no N. tenuis lated N. tenuis adults per day was not significantly developed successfully on tomato plants without prey different between both release rates, although more (Urbaneja et al. 2003a, b, 2005). Dicyphus hesperus nymphs were observed with the high rate. Prey Knight (Het.: Miridae) was also unable to complete availability per predator must have been lower at the its development when fed exclusively on tomato higher release rate, since the number of whitefly leaves (Gillespie and McGregor 2000). Conversely, nymphs was not significantly different. This would 123 244 J. Calvo et al.

Fig. 5 Observed and 5 empirical distribution based on a power model for the number of necrotic rings 4 caused by N. tenuis on depend of the prey 3 availability

2 Empirical: y = 15,086x-0,6359 Necrotic rings / leaf 1

0 0 500 1000 1500 2000 2500 3000 3500 Nymphs B. tabaci / N. tenuis (Adults + Nymphs)

OBSERVED Empirical result in reduced survivorship of mirid nymphs, either water from the plant for external digestion of prey directly through poorer nutrition or indirectly through (Gillespie and McGregor 2000). In contrast to both competitive interactions such as cannibalism, these mirids, D. tamaninii seems to damage tomato although our observations did not allow us to fruits independently of prey availability (model 3) distinguish between these possibilities. However, (Lucas and Alomar 2002). cannibalism in zoophytophagous species is not com- The ratio of B. tabaci nymphs and N. tenuis mon under field conditions (Castan˜e´ et al. 2002; individuals was the best predictor of incidence of Lucas and Alomar 2002). damage by N. tenuis. Therefore, to avoid undue The first necrotic rings surrounding the pedicel injury to a tomato crop by N. tenuis, special attention were detected on tomato leaves by week 6 of the test. should be paid to this ratio. Shipp and Wang (2006) The cumulative number of necrotic rings per leaf was observed that damage caused by D. hesperus significantly greater in the high release rate treatment. increased exponentially when a ratio of 1:10 (pre- Shipp and Wang (2006) in a similar trial also dator:prey) was exceeded. Alomar et al. (1991) came obtained a strong correlation between tomato damage to a similar conclusion for D. tamaninii preying on and prey availability when they tested different greenhouse whitefly Trialeurodes vaporariorum release rates of D. hesperus Knight (Het.: Miridae) (Westwood) (Hem: Aleyrodidae) in tomato green- against the western flower thrips, Frankliniella occi- houses. They recommended close monitoring of the dentalis (Pergande) (Thy.: Thripidae). relative abundance of predator and prey to avoid Gillespie and McGregor (2000) proposed three damage to tomato fruit (Lucas and Alomar 2002). simple models for feeding behaviour in omnivorous Alomar and Albajes (1996) provided a decision chart Heteroptera: (1) the amount of plant feeding indicating that insecticidal control against D. tama- decreases with increased prey feeding, (2) the amount nini was required when it exceeded 4 per plant and of plant feeding increases with increased prey feeding adult whitefly were less than 20 per plant. We and (3) the amount of plant feeding is independent of focused on whitefly nymphs rather than adults in our the amount of prey feeding. Nesidiocoris tenuis study, but could not provide a decision chart for appears to follow the first model because damage to N. tenuis because no information is available to relate tomato decreased in response to greater availability injury from this species to tomato yield or fruit of B. tabaci. These results agreed with those of Arno´ quality. When such information becomes available, et al. (2006) based on observations made under threshold ratios of B. tabaci nymphs to N. tenuis laboratory conditions. Hence, it seems that N. tenuis could be established. feeds on tomato plants when there is a lack of prey. This predator, like most mirid predators, displays a This behaviour differs from D. hesperus for which high degree of polyphagous behaviour and is able to damage to tomato increased in response to increased feed on several different pest species. Urbaneja et al. prey availability (model 2) due to the need to obtain (2003b, 2005) showed that on tomato leaves and 123 Predation by Nesidiocoris tenuis on Bemisia tabaci 245 under laboratory conditions at 25°C, N. tenuis was Cahill M, Gorman K, Day S, Denholm I, Elbert A, Nauen R able to complete its life cycle in 12.8, 13.21, 20.61 (1996) Baseline determination and detection of resistence to imidacloprid in Bemisia tabaci (Homoptera: Aleyro- and 23.44 days feeding on the eggs of E. kuehniella, didae). Bull Entomol Res 86:343–349 B. tabaci nymphs, larvae of F. occidentalis and Calvo J, Belda JE (2006) Comparacioń de estrategias de con- immatures and adults of Tetranychus urticae Koch trol biolo´gico de Bemisia tabaci Genn. (Homoptera: (Acari: Tetranychidae), respectively. Thus, the pre- Aleyrodidae) en pimiento en condiciones de semicampo. Bol Sanid Veg Plagas 32:297–311 sence of these other pests could potentially increase Calvo J, Urbaneja A (2003) Nesidiocoris tenuis (Het: Miridae) the tolerance level for N. tenuis per plant without en tomate: Amigo o Enemigo? Almerıá en Verde 4:21–23 significant increase in plant damage. Calvo J, Urbaneja A (2004) Nesidiocoris tenuis, un aliado para Mirid predators respond differently to different el control biolo´gico de la mosca blanca. Horticultura Internacional 44:20–25 plant types as well. For instance, D. tamaninii CARM (1996) El virus del rizado amarillo (hoja en cuchara) damages tomato but not cucumber (Gabarra et al. del tomate TYLCV y su vector Bemisia tabaci. Murcia. 1995; Castan˜e´ et al. 1996). Thus, the balance Consejerıá de Medio Ambiente, Agricultura y Agua de la between plant injury and biological control is deter- Regioń de Murcia, Murcia Carnero A, Dıáz S, Amador M, Hernańdez M, Hernańdez E mined by both the quantity and quality of plant and (2000) Impact of Nesidiocoris tenuis Reuter (Hemiptera: prey types (Eubanks and Denno 1997; Agrawal et al. Miridae) on whitefly populations in protected tomato 1999). As a consequence, the status of a mirid species crops. IOBC/WPRS Bull 23:259 such as N. tenuis as pest or biological control agent Castan˜e´ C (2002) Status of biological and integrated control in greenhouses vegetables in Spain: successes and chal- will depend on crop, pest complex, and possibly other lenges. IOBC/WPRS Bull 25(1):49–52 circumstances. Thus, further studies may be neces- Castan˜e´ C, Carnero A (2002) EWSN Release No 1. http:// sary to evaluate the utility of N. tenuis as biological www.whitefly.org/Resources/News/absolutenm/templates/ control agent in particular agroecosystems. NatEnemiesA4.asp?articleid=6&zoneid=14. Accessed 4 Feb 2007 Castan˜e´ C, Alomar O, Riudavets J (1996) Management Acknowledgments The authors thank Ana Gallego, Gervasio of western flower thrips on cucumber with Dicyphus Tapia and David Beltrań (Koppert B.S.; Spain) for technical tamaninii (Heteroptera: Miridae). Biol Control 7:114–120 assistance with experiments and maintenance of insect colonies. Castan˜e C, Iriarte J, Lucas E (2002) Comparison of prey This work was partially funded by the MCYT (Ministerio consumption by Dicyphus tamaninii reared conventio- Ciencia y Tecnologıá, Spain: Programa PROFIT) through nally, and on a meat-based diet. BioControl 47:657–666 project number of FIT-010000-2002-18. Dolling WR (1991) The Hemiptera. 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Inf Fitopatol 44:45–48 depredadores de intere´s para el control biolo´gico de Van der Blom J (2002) La introduccioń artificial de la fauna plagas en cultivos hortıćolas en la Regioń de Murcia. auxiliar en cultivos agrıćolas. Bol Sanid Veg Plagas Phytoma Espanã 154:55 28:109–120 Sańchez JA, del Pino-Pe´rez M, Davo´ MM, Martıńez-Cascales JI, Lacasa A (2006) Zoophytophagy of the plantbug Author Biographies Nesidiocoris tenuis in tomato crops in southeast Spain. IOBC/WPRS Bull 29:243–248 SIFA (2004) Servicio de informacioń Agraria. Junta de Andalucıá. Javier Calvo is an entomological researcher at Koppert B.S. http://desaveal.ual.es/sifa/inicio.htm. Accessed 4 Feb 2007 charged with evaluating biological control systems for Shipp JL, Wang K (2006) Evaluation of Dicyphus hesperus management of vegetable pests. (Heteroptera: Miridae) for biological control of Karel Bolckmans heads International R&D and production Frankliniella occidentalis (Thysanoptera: Thripidae) on activities of Koppert and is based at the Koppert headquarters greenhouse tomato. J Econ Entomol 99:414–420 in the Netherlands. Solsoloy AD, Domingo EO, Bilgera BU, Solsoloy TS, Begawan HS, Barluado ZD (1994) Occurrence, mortality factors and Philip A. Stansly conducts research and extension on pest within-plant distribution of bollworm, Helicoverpa armi- integrated management for the University of Florida and gera (Hu¨bn.) on cotton. Philipp J Sci 123:9–20 became involved in the project during a sabbatical year with SPSS (2004) SPSS v. 12 for windows. SPSS Inc., Chicago, IL Koppert B.S. Stansly PA, Sańchez PA, Rodrı´guez JM, Can˜izares F, Nieto A, Lo´pez MJ, Fajardo M, Sua´rez V, Urbaneja A (2004) Pros- Alberto Urbaneja is biological control specialist at the PVYB pects for biological control of Bemisia tabaci (Homoptera: of the Valencian Institute of Agricultural Research (IVIA, Aleyrodidae) in greenhouse tomatoes of Southern Spain. Spain) and previously worked as R&D manager at Koppert Crop Prot 23:710–712 B.S. in Spain. Stansly PA, Calvo J, Urbaneja A (2005a) Release rates for control of Bemisia tabaci (Homoptera: Aleyrodidae) 123